pearl aquaculture—profitable environmental remediation?

The Science of the Total Environment 319(2004) 27–37

0048-9697/04/$ - see front matter� 2003 Elsevier B.V. All rights reserved.doi:10.1016/S0048-9697(03)00437-6

Pearl aquaculture—profitable environmental remediation?

S. Gifford , R.H. Dunstan *, W. O’Connor , T. Roberts , R. Toiaa a, b,1 a a

School of Environmental and Life Sciences, University of Newcastle, Newcastle 2308, Australiaa

NSW Fisheries, Port Stephens Fisheries Centre, Taylors Beach, Australiab

Received 30 December 2002; accepted 11 July 2003

Abstract

Bivalve molluscs are filter feeders, with pearl oysters able to filter water at rates up to 25 l h g of dry wt.y1 y1

tissue. Since this process leads to rapid bioaccumulation of recalcitrant pollutants such as heavy metals, organochlorinepesticides and hydrocarbons from impacted sites, it has prompted the widespread use of molluscs as biomonitors toquantify levels of marine pollution. This paper proposes pearl oyster deployment as a novel bioremediation technologyfor impacted sites to remove toxic contaminants, reduce nutrient loads and lower concentrations of microbialpathogens. Estimates extrapolated from the literature suggest that a modest pearl oyster farm of 100 t oyster materialper year could remove 300 kg heavy metals plus 24 kg of organic contaminants via deposition into the tissue andshell. Furthermore, it was estimated that up to 19 kg of nitrogen may be removed from the coastal ecosystem pertonne of pearl oyster harvested. Pearl oysters are also likely to filter substantial amounts of sewage associatedmicrobial pathogens from the water column. Method of cultivation and site selection are the key to minimisingnegative environmental impacts of bivalve cultivation. Deployment of oysters at sites with high nutrient andcontaminant loadings would be advantageous, as these compounds would be removed from the ecosystem whilstgenerating a value-added product. Future potential may exist for harvesting bio-concentrated elements for commercialproduction.� 2003 Elsevier B.V. All rights reserved.

Keywords: Bioremediation; Pollutant cycling;Pinctada; Heavy metals; Water quality; Hydrocarbons; Bioaccumulation;Eutrophication

1. Introduction

Long-term risk chemicals that pollute the waterenvironment include heavy metals and recalcitrantsynthetic organics that can be derived from indus-

*Corresponding author. Tel.:q61-2-4921-5630; fax:q61-2-4921-7281.

E-mail address: [email protected](R.H. Dunstan).

Postal address: Private Bag 1, Nelson Bay, NSW 2315,1

Australia.

try, agriculture or domestic applications. Many ofthese are readily absorbed by animals and humansvia routes of ingestion, respiration or dermal expo-sure. Continued exposure to recalcitrant chemicalscan result in bioaccumulation of these contami-nants, particularly in fatty tissues, and biomagni-fication within the food chain(Nebel and Wright,1993). Other forms of pollution involve the exces-sive release of pathogenic organisms into theenvironment from human and animal sewage caus-ing potential health hazards, and the release of

28 S. Gifford et al. / The Science of the Total Environment 319 (2004) 27–37

high nutrient loads leading to eutrophication offreshwater and marine ecosystems. Thus, the chal-lenge for water authorities is to assess the leveland extent of contamination in waterways, min-imise toxic contaminant and nutrient loading, andcontrol sources of potential pathogen entry. Sincedilution of toxic compounds in coastal environ-ments makes direct measurements of contaminantloadings difficult, bivalves are commonlyemployed as biomonitors of marine pollution(Phillips and Rainbow, 1993). This is a directreflection on the capacity of bivalves to filter largevolumes of water(25 l h g , Pouvreau et al.,y1 y1

1999) and bioaccumulate various xenobiotics toanalytically detectable levels.

Bioremediation is usually confined to processesemploying microorganisms or plants to break downtoxic chemicals in the environment(Baker andHerson, 1994). The use of animal systems asbioremediators has not been seriously consideredin the past, due to ethical reasons or because theend products are associated with human consump-tion. The use of pearl oysters as bioremediators inappropriate environments is attractive since themarket value lies with the pearl and not the flesh.The tissue is not necessarily utilised for human oranimal consumption and issues of health biohaz-ards are not relevant. The oysters would be usedto filter large volumes of water to remediatestressed coastal environments whilst forming a newpearl. This represents a novel application of ananimal system to bioremediation with high poten-tial commercial gain.

Several characteristics of pearl oysters supporttheir use as bioremediators. Firstly, the cosmopol-itan distribution of the various species of pearloysters, such asPinctada imbricata (Colgan andPonder, 2002), allows the luxury of selecting anendemic organism for remediation in many areasof the world. Secondly, the volume of waterpumped by pearl oysters is the highest of anybivalve, with the pumping rate of the black lippearl oyster,Pinctada margaritifera, reported at25 l h g dry wt. of oyster soft tissue(Pouvreauy1 y1

et al., 1999). Thirdly, pearl oyster tissue has a highprotein content, compared to other bivalves, andtherefore cultured pearl oysters have a good poten-

tial capacity to remediate nutrient loads at thesame time as toxic chemical loads.

For the purpose of this review, a model pearlfarm harvesting 100 t(wet wt.) of oysters per yearis used for calculating remediation potential. Thisrepresents approximately 40 t soft tissue(10 t drywt.) and 60 t shell material. However, it shouldbe noted that commercial bivalve operations aregenerally larger than this. For example, in 1990harvests from farm areas totalled 200 000 t inGalicia, NW Spain(Navarro et al., 1991) and73 000 t in Hiroshima Bay, Japan(Songsangjindaet al., 2000). Ultimately, the scale of farmingoperations will determine the amount of pollutantsor nutrients removed by any specific pearlingoperation. Through application of the highestreported concentrations of pollutants and nutrientsin the shell and soft tissue of many species ofbivalves to the pearl farm model, this paperreviews the potential for pearl oysters to be usedin bioremediation of pollution impacted marinesights. Specifically, this review discusses the bioac-cumulation of heavy metals and organopollutants,the lowering of nutrient loads and possible reme-diation of sewage associated microbial pathogensby pearl oysters. Finally, a review of the potentialdeleterious effects of large-scale bivalve cultiva-tion is included.

2. Bioaccumulation of pollutants

2.1. Heavy metals

Heavy metals are used widely in industry andcan enter the environment via low-dose continualinflux. Over time this can lead to significant‘enrichment’ of ecosystems via bioaccumulationin plankton and filter feeders and biomagnificationthrough the food chain. Heavy metals may damagebiological systems by replacing essential metals ascofactors, inhibiting enzymes, altering membraneintegrity and causing physiological damage. Manyorganisms have evolved mechanisms to deal withtoxic metal loads, but these biological systems canbecome stressed and overloaded leading to cellulardamage, usually via oxidative processes.

The degree of uptake and storage of heavymetals in oyster soft tissue is controlled by many

29S. Gifford et al. / The Science of the Total Environment 319 (2004) 27–37

Table 1The potential for removal from the aquatic environment of selected pollutants was estimated by the extrapolation of publishedbioaccumulation data for a hypothetical 100 t pearl oyster farm

Pollutant Amount removed

Soft tissue(g) Shell (g)

Cu 20 130 Oliver et al.(2001)5 1500 Richardson et al.(2001)8

Zn 90 770 Oliver et al.(2001)5 2100 Richardson et al.(2001)8

Fe 50 000 Peerzada and Kozlik(1992)3 55 344 Al-Aasm et al.(1998)13

Pb 5058 Bourgoin(1990)7 5766 Al-Aasm et al.(1998)10

Ni 134 Oliver et al.(2001)5 1428 Almeida et al.(1998a)9

As 730 Fowler et al.(1993)1 96 Cheung and Wong(1992)6

Cd 1080 Francesconi(1989)12 836 Cheung and Wong(1992)6

Cr 288 Fowler and Oregioni(1976)2 366 Almeida et al.(1998a)9

Al 22 400 Sbriz et al.(1998)4 24 588 Prakash and Rao(1993)6

Sr Not reviewed 51 000 Almeida et al.(1998a)9

Mn Not reviewed 31 200 Frazier(1976)5

OC 28 Oliver et al.(2001)5 Not reportedPAH 7600 Villeneuve et al.(1999)2 Not reportedTH 13 000 Villeneuve et al.(1999)2 3130 Walsh et al.(1995)11

Values given do not represent the maximum potential limit of pollutant removal as all values represent site-specific pollutantloadings. OC, organochlorines; PAH, polyaromatic hydrocarbons; TH, total hydrocarbons. Organism used in cited reference(1)Pinctada margaritifera, (2) Mytilus galloprovincialis, (3) Saccostrea sp., (4) Crassostrea rhizophorae, (5) Crassostrea virginica,(6) Perna viridis, (7) Mytilus edulis, (8) Modiolus modiolus, (9) Crassostrea gigas, (10) Dreissena polymorpha, (11) Austrocochleaconstricta, (12) Pinctada albina albina. As an example, the calculations for Cu are as follows:Soft tissue: Oliver et al. (2001)reported the value of 2013mg g dry wt. for copper at St. Andrews Bay. On a per tonne basis, this figure becomes 2013 g t .y1 y1

Given our 100 t model pearl farm is generating 10 t of dry wt. soft tissue material, the value reported by Oliver et al.(2001) wasmultiplied by 10, giving the value presented.Shell material: Richardson et al.(2001) reported the value of 25 mg kg Cu or 25y1

g t . Given our 100 t model pearl farm is generating 60 t of shell material, the value reported by Richardson et al.(2001) wasy1

multiplied by 60, giving the value presented.

factors including size, age, sex, season, contami-nant interactions, salinity, water temperature and,most importantly, degree of localised pollution(Phillips and Rainbow, 1993). Furthermore, this isa dynamic process, reflecting the surrounding envi-ronmental load. For example, transference of oys-ters from polluted to clean water is commonlyused to allow depuration of metals from soft tissue(Chan et al., 1999). This attribute of the oystersmakes them useful as biomonitors reflectingchanges in contaminant loads in marineenvironments.

On the basis of published data from oysterssampled from contaminated environments, theamounts of heavy metals measured in the tissueswere extrapolated to the 100 t pearl farm scenarioas shown in Table 1. These data demonstrate thatpearl farming has the ability to remove kilogramquantities of metals solely through uptake andstorage in soft tissue of the oysters. Although the

highest removal capacities indicated are lead, alu-minium, copper, zinc and iron, it must be notedthat the data only reflect the specific environmentfrom which the organisms were sampled from.Other metals may well be accumulated if presentin high quantities(Table 1). At present it is notknown what toxic loads these organisms can bearbefore their metabolism is adversely affected norwhether bioaccumulation of heavy metals in thetissue affects pearl production. Similarly, the ques-tion of disposal of harvested contaminated oystertissues also needs to be addressed.

In addition to bioaccumulation of contaminantsin the soft tissue, bivalves may also incorporatemetals within their shell matrix during the processof biomineralisation. This process occurs in twodistinct ways. Either metals may be included with-in the organic matrix that binds the various bivalveshell layers, or metals with an ionic radius similarto calcium may directly occupy a place within the


calcium carbonate matrix of the shell(Lingard etal., 1992). Unfortunately, research investigatingbioaccumulation of heavy metals in bivalve shellsis scarce compared with that in bivalve soft tissues.Nonetheless, levels of heavy metals within theshell matrix have been reported for severalbivalves including clams, mussels and some spe-cies of oysters, but not pearl oysters(Segar et al.,1971; Bertine and Goldberg, 1972; Sturesson,1976, 1978; Cheung and Wong, 1992; Prakash andRao, 1993; Pitts and Wallace, 1994; Puente et al.,1996; Al-Aasm et al., 1998; Almeida et al.,1998a,b; Huanxin et al., 2000; Richardson et al.,2001; Wiesner et al., 2001). Most heavy metals ofindustrial relevance and toxicological concern havebeen measured in the shell matrices, and somevalues indicate substantial capacity for deposition,including Al, Fe, Mn, Sr and Pb. The depositionof metals in shells may function as a detoxifyingmechanism for the animal(Bertine and Goldberg,1972; Sturesson, 1978; Al-Aasm et al., 1998),where the appropriate elements are ‘locked’ intothe shell matrix, physically separating them fromtissues with active metabolism.

On the basis of the available data, it appearsthat levels of depuration of metals in the shells ofbivalves are negligible compared with soft tissues(Sturesson, 1978; Bourgoin, 1990; Puente et al.,1996). Application of this has allowed the assess-ment of metal loadings from fossilised samples(Pitts and Wallace, 1994). This is of great interestas a potential bioremediation system because theheavy metals are effectively removed from thefood chain when deposited into the shell, even ifthe shells form part of the benthos as in wildmolluscan populations. In the case of cultivatedbivalves, the shells are removed from the ecosys-tem and the potential may even exist to ‘mine’ themetals from the shell matrix. As was done abovefor the soft tissues, literature values from bioac-cumulation studies on the shell matrix have beenextrapolated to the 100 t pearl farm scenario inTable 1. These data give an indication of the greatpotential for heavy metal removal from coastalsystems via the shell of cultivated molluscs. Fur-thermore, through consideration of the great num-bers of molluscs of the world’s coasts, it issuggested that bivalves play an important role in

natural ecosystems in maintaining homeostasis inmetal loading of the aqueous environment. Bymolluscan shells effectively acting as a pollutantsink (Bertine and Goldberg, 1972; Sturesson,1978; Walsh et al., 1995; Al-Aasm et al., 1998)coastal ecosystems may be buffered against epi-sodic events of coastal metal input.

No investigations could be found in the Englishlanguage scientific literature describing the ele-mental composition of actual pearls. Given thatthe shell nacre and the layers of material formingthe pearl are identical, it is proposed that thecomposition of the pearl includes heavy metalsand trace elements, and that the process of pearlformation may be an elaborate mechanism of toxicelement removal. Laboratory based investigationsof the physiology of heavy metal deposition inpearl oysters into the shell and pearl matrices arerequired to fully evaluate the full potential of pearloysters as bioremediator organisms.

2.2. Organopollutants

The recalcitrant synthetic organic pollutantsentering the marine environments include somepesticides, PCBs, halogenated compounds andpetroleum hydrocarbons. These compounds areused widely in industrial, agricultural and domesticapplications. Because these pollutants are recalci-trant, they may accumulate in fatty tissues andbiomagnify throughout the food chain. Someindustrial by-products such as dioxins are extreme-ly toxic, and other organic pollutants, such assolvents, are rapidly degraded but cause damagethat can have long lasting impacts on the metabo-lism and survivability of exposed animals in eco-systems. Many organic pollutants arise fromsurface run-off and storm-water entry into coastalsystems, atmospheric deposition, as well as contri-butions of petroleum products from industrial andrecreational boating.

Organopollutants entering the marine environ-ment are immediately diluted, often making anal-ysis difficult. Since organochlorines and hydro-carbons accumulate in the soft tissue of bivalves,these organisms have been used to assess organicpollutant loadings in marine environments(Phil-lips and Rainbow, 1993). Large data sets exist


from both the ‘mussel watch program’ of the 1970sand its replacement, the National Status and TrendsProgram of the National Oceanic and AtmosphericAdministration(NOAA) in the Americas(Serica-no et al., 1995). As well as using bivalves todirectly quantify organic pollutant loadings, theeffect on the oyster physiology following deploy-ment into pollution-impacted sites has also beenstudied(Avery et al., 1998). These authors showedthat the oysters’ membrane composition alterssignificantly in response to the local environments,allowing polluted sites to be identified even whenunsure of target pollutants.

Literature values of soft tissue bioaccumulationstudies from contaminated environments have beenextrapolated to the 100 t pearl farm scenario inTable 1, and demonstrate the capacity for removalof significant amounts of hydrocarbons. In areasof industry or high proximate boating traffic, thiswould assist in the removal of petroleum hydro-carbons from the coastal environment. Whilst thevalues for organochlorines were low, this reflectsthe pesticide loading of the local environment fromwhich the data were generated. Further work isrequired to investigate the potential for removal ofthese recalcitrant pollutants as well as to determinethe tolerance levels of the oysters under in vitroconditions.

Only one published data set was found fororganic contaminants in the mollusc shell matrix(Walsh et al., 1994, 1995). These authors proposedthat those compounds resistant to degradation viathe cytochrome P450 pathway may be excretedthrough the extrapallial fluid to be incorporatedinto the shell matrix, utilising the shell as aneffective pollutant sink. This is demonstrated viathe fact thatAustrocochlea constricta accumulatedC14–C18 aliphatic hydrocarbons in the soft tissuewhere they can be detoxified or tolerated butlonger chain (C20–C30) hydrocarbons weredeposited within the shell matrix(those com-pounds resistant to degradation). This suggeststhat molluscs have a much more sophisticatedresponse to organopollutant challenge than previ-ously thought. While organopollutants are oftenlipohillic and shells are typically not thought tocontain significant quantities of organic matter, thepossibility exists for both the proteinaceous perios-

tracum and the organic matrix binding the calciticand aragonitic layers of the shell to accumulateorganopollutants. Ecologically, further research isclearly warranted to determine the capacity forbivalves to deposit organic contaminants into theshell matrix, as compounds deposited in this man-ner would be effectively removed from the foodchain.

3. Nutrient cycling and water quality issues

Increasing coastal urbanisation and industrialis-ation combined with modern farming techniqueshas, in some areas, led to excess input of nutrientsinto coastal ecosystems. Increasing nutrient loadscan have several impacts, most notably the stimu-lation of primary production. The subsequent deathof these increased phytoplankton communitiesoften leads to a depletion of dissolved oxygenlevels in the water column. These eutrophic coastalareas, characterised by a high nutrient-low dis-solved oxygen chemical signature, may have manycascading ecological effects, including fish kills.

The role of wild bivalve stocks in the nutrientcycle has, as such, been extensively studied, withthe view of potentially using them to increasenutrient cycling and relieve eutrophication pres-sures on coastal ecosystems(Officer et al., 1982;Asmus and Asmus, 1991). The nutrient cyclingcapabilities of bivalves will, of course, improveexponentially when the mature organisms areextracted and replaced with rapidly growing juve-niles, as is the case in aquaculture(Songsangjindaet al., 2000). Typically, the protein content ofbivalves varies between 40 and 50% of the softtissue dry wt.(Miletic et al., 1991; Linehan et al.,1999). However, since the protein content of pearloysters is amongst the highest of any bivalvespecies, with values up to 88.02% of dry tissue asprotein (Suzuki, 1957), the nitrogen harvest pertonne of pearl oyster meat is likely to be amongthe most efficient of the bivalves. Table 2 lists theextrapolated nitrogen removed by the 100 t pearlfarm and the data suggest that more than 1 t ofnitrogen could be removed from the coastal systemwith each harvest solely through the soft tissue(Suzuki, 1957; Seki, 1972; Numaguchi, 1995).Additional nitrogen is removed via the shell(Goul-


Table 2The potential for removal from the aquatic environment of nutrients was estimated by the extrapolation of publishedelementalyprotein composition data for a hypothetical 100 t pearl oyster farma

Literature source Species Shellytissue Nutrient (kg)

P N

Yamamuro et al.(2000) Musculista senhousia Shell 41 528Goulletquer and Wolowicz(1989) Ruditapes philippinarum Shell nm 62Westermark et al.(1996a) M. margaritifera Shell 6 426Seire et al.(1996) Macoma baltica Shell 17 63Westermark et al.(1996b)b Arctica islandica L. Shell 2 30Nakamura et al.(1988) Corbicula japonica Shell nm 132Rice (2001)c generic Tissue nm 336Songsangjinda et al.(2000)d Crassostrea gigas Tissue nm 1390Miletic et al. (1991) M. galloprovincialis Tissue nm 620Miletic et al. (1991) Venus verucosa Tissue nm 684Linehan et al.(1999)e Crassostrea gigas Tissue nm 743Numaguchi(1995)f Pinctada imbricata Tissue nm 1030Seki (1972)f,g Pinctada imbricata Tissue nm 1022Suzuki(1957)h,i Pinctada imbricata Tissue nm 1232Cantoni et al.(1977) Mytilus edulis Tissue 82 549Sidwell et al.(1973) C. virginica Tissue 58 323Oishi et al.(1970) Pecten yessoensis Tissue 123 1330

As an example, the phosphorus calculation for Yamamuro et al.(2000) is given: the reported shell value of 0.675 mg g equatesy1

to 0.675 kg t . Given our 100 t model pearl farm is generating 60 t of shell material, this value was multiplied by 60, giving they1

value presented. nm, not measured.Protein was converted to %N via multiplying by 0.14(Rice, 2001).a

Highest ‘most probable range’ value used.b

Published value of 16.8 g t N tissue has since been revised to 8.4 g t N tissue(Rice, personal communication).c y1 y1

N t value used(dw) and multiplied by 10.d y1

August value used.e

Average protein content of 73% dry meat wt.f

June value of protein content used.g

Reported asPinctada fucata, see Colgan and Ponder(2002).h

Reported asPinctada martensii, see Colgan and Ponder(2002).i

letquer and Wolowicz, 1989; Inoue and Yamamu-ro, 2000). Substantial levels of phosphorous werealso removed via harvest of mollusc soft tissues(Oishi et al., 1970; Sidwell et al., 1973; Cantoniet al., 1977) and shells(Inoue and Yamamuro,2000).

While nutrient removal through commercialbivalve operations has scarcely been studied(Rice,2001), reduction in water column chlorophyllaconcentrations by bivalves is well documented(Riemann et al., 1988; Beaver et al., 1991; Dameet al., 1991; Shpigel and Blaylock, 1991; Phelps,1994; Nakamura and Kerciku, 2000; Jones et al.,2002). For example, between 1988 and 1989,following the introduction of the zebra mussel inLake Erie, chlorophylla concentrations reduced

by 43%, and mean sechi disc transparenciesincreased by 1.24 m(Leach, 1993). Similar resultshave been reported for this species in Holland,where the use of this organism within water qualitymanagement programs has been successfully trial-led (Reeders et al., 1993; Smit et al., 1993).Similarly, dense beds of the musselMytilus edulisactively recycle nutrients in coastal systems(Dameet al., 1991), and significantly reduce levels ofphytoplankton in the water column(Riemann etal., 1988).

Ecologically, filter feeders play an importantrole in coastal ecosystems. Following the estab-lishment of large numbers of the Asiatic clam(Corbicula fluminea) in the Potomac River estuaryin the early 1980s, substantial improvements in


water quality were observed coinciding with thereappearance of submerged aquatic vegetationwhich had been absent for 50 years(Phelps, 1994).Fish surveys also revealed large increases in fish-eries populations, while large increases in thepopulations of several aquatic bird species werealso reported. The importance of this ‘top down’pressure exerted by bivalves within coastal ecosys-tems is being increasingly recognised, with oysterreef habitat areas now an important conservationissue(Coen and Luckenbach, 2000). The role ofoyster reef habitat in coastal ecosystems is likelymimicked by commercial bivalve operations.

A major water quality issue for freshwater andmarine environments is the influx of bacteria,viruses and protozoans from human and animalwaste. This may have specific relevance for coastalcommunities where potential pathogens enter watersystems via sewage outfalls, accidental spillageand discharge from boats, overload from septicsystems during high rainfall events, agriculturalpractice and input from native animal species.There is concern for existing oyster farms growingflesh for human consumption that pathogenic load-ing may render their produce unacceptable forsale. Production of pearl oysters is not restrictedby bacterial loading of the environment since theend product is not consumed. There are somereports in the literature indicating that differentbivalve species can utilise bacteria as food sourcesat varying rates and thus potentially reduce coli-form levels in marine environments(McHenery etal., 1979; McHenery and Birkbeck, 1985; Silver-man et al., 1995). Briefly, the main factor influ-encing the retention efficiency of bacteria bybivalves is the presence of eu-latero frontal cirrion the gills(Silverman et al., 1995). It is importantto note, however, that the majority of these studieshave focused on the bivalves ability to utilisebacteria as a food source, rather than the bivalvesability to remove bacteria from the water column.Importantly, if bacteria are trapped within themucus and are rejected as pseudofaeces, implyingthey are not digested by the bivalve, this may stillresult in the destruction and sedimentation ofbacteria, effectively removing them from the watercolumn (Bernard, 1989). As such, determinationsof the capacity of pearl oysters to be used to

remove microscopic pathogenic organisms fromthe water column need to incorporate both directlydigested and pseudofaeces bound bacteria by theoyster. While reported usage of microorganismsby pearl oysters is scarce, Pouvreau et al.(1999)reported that the black lip pearl oyster retainsapproximately 50% of particles 2mm in size,falling to approximately 15% for particles 1mmin size. The particles used in this study were,however, all algae. Recently, the importance of thehydrophobic nature of some bacteria in relation toparticle retention efficiency has been demonstrated(Llanos and Garcia-Tello, 2000). These authorsshowed that retention efficiency of the hydropho-bic bacteriaSalmonella paratyphi, Staphylococcusaureus and Vibrio cholerae by the bivalveMeso-desma donacium was significantly greater than forthe hydrophilic bacteriumAeromonas hydrophila.Given these factors, the removal of pathogenicmicroorganisms by bivalves is likely to be speciesspecific for both the bivalve and the pathogen.Research is required to ascertain whether key pearloyster spp. can be used to reduce pathogeniccontaminants from sewage-impacted sites.

4. Impact of shellfish aquaculture

The abilities of bivalves to decrease turbidity,control eutrophication, lower concentrations ofbacterial pathogens and remove toxic chemicalsare powerful arguments in favour of their deploy-ment. However, the impact of introducing speciesto pollution-impacted sites warrants close investi-gation to ensure that a significant adverse impactis not triggered. Previous studies have consideredthe release of ‘free-range’ bivalves for remediationpurposes. Intensive aquaculture of edible bivalvesfor bioremediation would be cost intensive as theflesh would be unacceptable for human consump-tion unless nutrient removal was the sole objective.However, the use of pearl oysters for bioremedia-tion would be commercially viable because thevalue-added product can be sold irrespective oftissue levels of contaminants.

High-density commercial pearl farms canadversely impact marine ecosystems, due to theshear volume of biomatter processed by the ani-mals. The most commonly reported environmental


impact of commercial bivalve aquaculture sites isincreased sedimentation, as a result of biodeposi-tion of faecal and pseudofaecal material, belowlease areas(Dahlback and Gunnarsson, 1981; Kas-par et al., 1985; Grenz et al., 1990; Hatcher et al.,1994; Grant et al., 1995; Stenton-dozey et al.,1999; Souchu et al., 2001). No data exist forequivalent investigations of pearl farms. Severalpoints of criticism can be made in the design ofthese studies by focussing on the use of only onecontrol site and a lack of site evaluation beforeand after establishment of the aquaculture lease.

The lack of proper ecological design has plaguedthe field of environmental impact assessment(Fairweather, 1989; Underwood, 1992, 1995; War-wick, 1993). The great majority of reportedimpacts of shellfish culture relied on one controlsite (Dahlback and Gunnarsson, 1981; Kaspar etal., 1985; Grenz et al., 1990; Hatcher et al., 1994;Grant et al., 1995; Souchu et al., 2001). Variabilityin the marine environment is striking, and ifseveral locations within a pristine bay, for example,with no anthropogenic inputs were sampled, thevariation between sites is likely to be large(Under-wood, 1992, 1995). As such, it is difficult toestablish whether the variation between one controlsite and a bivalve farm is due to impacts by thebivalves, or is merely natural variation within thelocal system. Future work into the environmentalimpacts of commercial bivalve operations(orindeed any marine development) must incorporatenatural ecosystem variation within the experimen-tal design, preferably utilising the beyond BACIexperimental design protocol(Underwood, 1992).

Recent investigations have concluded that it is,in fact, the build up of displaced cultured organ-isms, fouling algae or ascidians beneath long-lineculture sites that have more of an impact on thebenthos than bivalve biodeposition(Stenton-dozeyet al., 1999). In the case of long-line pearl oysteroperations, the pearl oyster is significantly morevaluable than edible bivalves. As such, they arekept in bags hanging from the long line to preventloss of the organism. This bag must, however, becleaned regularly to remove fouling organisms sothat water flow is maintained to the oysters. Tofacilitate this, a boat runs along the long line andthe oyster bags are brought aboard, with fouling

communities removed and, in best-practice opera-tions, disposed of ashore. Accordingly, the effectsof both displaced bivalves and fouling organismson the benthos below the lines would appear to bespecific to edible bivalves and not of particularconcern to best-practice pearling operations.

The majority of farm sites studied occurred inareas with little or no tidal flushing and very lowcurrent speeds(Dahlback and Gunnarsson, 1981;Hatcher et al., 1994; Grant et al., 1995; Souchu etal., 2001). Chamberlain et al.(2001) demonstratedthat in mussel cultivation, the benthos of a sitewith tidal flushing was negligibly impacted butthe benthos of a site with little tidal flushing hadsignificant impacts. The issue of site selection withappropriate depth characteristics and tidal flushingwould comprise important considerations for thelong-term deployment of pearl oysters as biore-mediators. However, if a site is heavily polluted,then such deployment issues must be weighedagainst the potential gain of site remediation.

5. Conclusion

The use of pearl oysters for bioremediation hashigh potential since published data indicate thatthey have a high capacity to remove significantquantities of heavy metals, organopollutants andnutrients from the surrounding marine environ-ment. This would lead to a direct improvement inwater quality. The use of pearl oysters as opposedto edible oysters means that the process of biore-mediation would have a highly value-added com-mercial return that is not restricted by issues relatedto human consumption. It is also possible thatfuture technologies may allow the harvest of bio-concentrated rare elements for commercial produc-tion. When best-practice operations are utilised,combining low stocking densities, removal of foul-ing organisms and subsequent on-shore disposal,the potential for deleterious environmental effectsis likely to be minimal. Future studies should beaimed at investigating the effects of bioaccumula-tion of pollutants on pearl production and deter-mine the tolerance limits for selected pearl oysters.The investigation of the capacity for pearl oystersto utilise coliform bacteria may also lead to newrealms of bioremediation for coastal communities.


Site selection criteria of pearling operations shouldbe expanded to include current velocities, andcould include targeting areas of chronic pollutionand coastal anthropogenic nutrient input. Thedetoxifying role of the molluscan shell, and itsoverall pollutant cycling capabilities within thecontext of the ecosystem at large, would also profitfrom extended research.

References

Al-Aasm IS, Clarke JD, Fryer BJ. Stable isotopes and heavymetal distribution inDreissena polymorpha (zebra mussels)from western basin of Lake Erie, Canada. Environ Geol1998;33:122–129.

Almeida MJ, Machado J, Moura G, Azevedo M, Coimbra J.Temporal and local variations in biochemical compositionof Crassostrea gigas shells. J Sea Res 1998;40:233–249.

Almeida MJ, Moura G, Pinheiro T, Machado J, Coimbra J.Modifications in Crassostrea gigas shell compositionexposed to high concentrations of lead. Aqua Tox1998;40:323–334.

Asmus RM, Asmus H. Mussel beds: limiting or promotingphytoplankton. J Exp Mar Biol Ecol 1991;148:215–232.

Avery EL, Dunstan RH, Nell JA. The use of lipid metabolicprofiling to assess the biological impact of marine sewagepollution. Arch Environ Contam Toxicol 1998;35:229–235.

Baker K, Herson D. Bioremediation. New York: McGraw-Hill,1994.

Beaver JR, Crisman TL, Brock RJ. Grazing effects of anexotic bivalve(Corbicula fluminea) on hypereutrophic lakewater. Lake Reservoir Manage 1991;7:45–51.

Bernard FR. Uptake and elimination of coliform bacteria byfour marine bivalve mollusks. Can J Fish Aquat Sci1989;46:1592–1599.

Bertine KK, Goldberg ED. Trace elements in clams, mussels,and shrimp. Limnol Oceanogr 1972;17:877–884.

Bourgoin BP.Mytilus edulis shell as a bioindicator of leadpollution considerations on bioavailability and variability.Mar Ecol Prog Ser 1990;61:253–262.

Cantoni C, Cattaneo P, Ardemagni A. A report on P contentin fleshes of aquatic animals(in Italian). Industrie Alimen-tari 1977;16:89–90.

Chamberlain J, Fernandes TF, Read P, Nickell TD, Davies IM.Impacts of biodeposits from suspended mussel(Mytilusedulis L.) culture on the surrounding surficial sediments.ICES J Mar Sci 2001;58:411–416.

Chan KW, Cheung RYH, Leung SF, Wong MH. Depurationof metals from soft tissues of oysters(Crassostrea gigas)transplanted from a contaminated site to clean sites. EnvironPollut 1999;105:299–310.

Cheung YH, Wong MH. Comparison of trace metal contentsof sediments and mussels collected within and outside ToloHarbour, Hong Kong. Environ Manage 1992;16:743–751.

Coen LD, Luckenbach MW. Developing success criteria andgoals for evaluating oyster reef restoration: ecological func-tion or resource exploitation. Ecol Eng 2000;15:323–343.

Colgan DJ, Ponder WF. Genetic discrimination of morpholog-ically similar, sympatric species of pearl oysters(Mollusca:Bivalvia: Pinctada) in eastern Australia. Mar FreshwaterRes 2002;53:697–709.

Dahlback B, Gunnarsson LAH. Sedimentation and sulfatereduction under a musselMytilus edulis culture. Mar Biol1981;63:269–276.

Dame R, Dankers N, Prins T, Jongsma H, Smaal A. Theinfluence of mussel beds on nutrients in the western WaddenSea and eastern Scheldt Estuaries. Estuaries 1991;14:130–138.

Fairweather PG. Environmental impact assessment; where isthe science in EIA? Search 1989;20:141–144.

Fowler SW, Oregioni B. Trace metals in mussels from the NWMediterranean. Mar Pollut Bull 1976;7:26–29.

Fowler SW, Readman JW, Oregioni B, Villeneuve J-P, McKayK. Petroleum hydrocarbons and trace metals in nearshoreGulf sediments and biota before and after the 1991 war: anassessment of temporal and spatial trends. Mar Pollut Bull1993;27:171–182.

Francesconi KA. Distribution of cadmium in the pearl oyster,Pinctada albina albina (Lamarck), following exposure tocadmium in seawater. Bull Environ Contam Toxicol1989;43:321–328.

Frazier JM. The dynamics of metals in the American oyster,Crassostrea virginica. 2. Environmental effects. Ches Sci1976;17:188–197.

Goulletquer P, Wolowicz M. The shell ofCardium edule,Cardium glaucum and Ruditapes philippinarum organiccontent composition and energy value as determined bydifferent methods. J Mar Biol Assoc UK 1989;69:563–572.

Grant J, Hatcher A, Scott DB, Pocklington P, Schafer CT,Winters GV. A multidisciplinary approach to evaluatingimpacts of shellfish aquaculture on benthic communities.Estuaries 1995;18:124–144.

Grenz C, Hermin M-N, Baudinet D, Daumas R. In situbiochemical and bacterial variation of sediments enrichedwith mussel biodeposits. Hydrobiologia 1990;207:153–160.

Hatcher A, Grant J, Schofield B. Effects of suspended musselculture (Mytilus spp.) on sedimentation, benthic respirationand sediment nutrient dynamics in a coastal bay. Mar EcolProg Ser 1994;115:219–235.

Huanxin W, Lejun Z, Presley BJ. Bioaccumulation of heavymetals in oyster(Crassostrea virginica) tissue and shell.Environ Geol 2000;39:1216–1226.

Jones AB, Preston NP, Dennison WC. The efficiency andcondition of oysters and macroalgae used as biologicalfilters of shrimp pond effluent. Aquacult Res 2002;33:1–19.

Kaspar HF, Gillespie PA, Boyer IC, Mackenzie AL. Effects ofmussel aquaculture on the nitrogen cycle and benthic com-munities in Kenepuru Sound Marlborough Sounds New-Zealand. Mar Biol 1985;85:127–136.


Leach JH. Impacts of the zebra mussel(Dreissena polymor-pha) on water quality and fish spawning reefs in westernLake Erie. In: Nalepa TF, Schloesser DW, editors. Zebramussels: biology, impacts, and control. Boca Raton, FL:Lewis Publishers, 1993. p. 381–397.

Linehan LG, O’Connor TP, Burnell G. Seasonal variation inthe chemical composition and fatty acid profile of Pacificoysters(Crassostrea gigas). Food Chem 1999;64:211–214.

Lingard SM, Evans RD, Bourgoin BP. Method for the esti-mation of organic-bound and crystal-bound metal concentra-tions in bivalve shells. Bull Environ Contam Toxicol1992;48:179–184.

Llanos J, Garcia-Tello P. Role and behaviour of the hydropho-bic conditions in bacterial adhesion to incurrent siphon in abivalve mollusc. Acta Microbiol Pol 2000;49:75–82.

McHenery JG, Birkbeck TH. Uptake and processing of cul-tured microorganisms by bivalves. J Exp Mar Biol Ecol1985;90:145–163.

McHenery JG, Birkbeck TH, Allen JA. The occurrence oflysozyme in marine bivalves. Comp Biochem Physiol, B:Comp Biochem, Part B 1979;63:25–28.

Miletic I, Miric M, Lalic Z, Sobajic S. Composition of lipidsand proteins of several species of molluscs, marine andterrestrial, from the Adriatic Sea and Serbia. Food Chem1991;41:303–308.

Nakamura M, Yamamuro M, Ishikawa M, Nishimura H. Roleof the bivalveCorbicula japonica in the nitrogen cycle ina mesohaline lagoon. Mar Biol 1988;99:369–374.

Nakamura Y, Kerciku F. Effects of filter-feeding bivalves onthe distribution of water quality and nutrient cycling in aeutrophic coastal lagoon. J Mar Sys 2000;26:209–221.

Navarro E, Iglesias JIP, Perez Camacho A, Labarta U, BeirasR. The physiological energetics of mussels(Mytilus gallo-provincialis Lmk) from different cultivation rafts in the Riade Arosa(Galicia, NW Spain). Aquaculture 1991;94:197–212.

Nebel BJ, Wright RT. Environmental science. New Jersey:Prentice Hall, 1993.

Numaguchi K. Effects of water temperature on catabolic lossesof meat and condition index of unfed pearl oysterPinctadafucata martensii. Fish Sci 1995;61:735–738.

Officer CB, Smayda TJ, Mann R. Benthic filter feeding: anatural eutrophication control. Mar Ecol Prog Ser1982;9:203–210.

Oishi K, Lida A, Yoshimura A. Amino acid composition andphosphorous content in extracts of scallop abductor muscle.Bull Jap Soc Sci Fish 1970;36:1226–1230.

Oliver LM, Fisher WS, Winstead JT, Hemmer BL, Long ER.Relationships between tissue contaminants and defense-related characteristics of oysters(Crassostrea virginica)from five Florida bays. Aqua Tox 2001;55:203–222.

Peerzada N, Kozlik E. Seasonal variation of heavy metals inoysters from Darwin Harbor, Northern Territory, Australia.Bull Environ Contam Toxicol 1992;48:31–36.

Phelps HL. The Asiatic clam(Corbicula fluminea) invasionand system-level ecological change in the Potomac RiverEstuary near Washington, DC. Estuaries 1994;17:614–621.

Phillips D, Rainbow P. Biomonitoring of trace aquatic contam-inants. London, New York: Elsevier Applied Science, 1993.

Pitts LC, Wallace GT. Lead deposition in the shell of thebivalve, Mya arenaria: an indicator of dissolved lead inseawater. Estuar Coast Shelf Sci 1994;39:93–104.

Pouvreau S, Jonquieres G, Buestel D. Filtration by the pearloyster, Pinctada margaritifera, under conditions of lowseston load and small particle size in a tropical lagoonhabitat. Aquaculture 1999;176:295–314.

Prakash TJ, Rao KSJ. Relationship between the metal contentin bivalve shell and its physical parameters. FreseniusEnviron Bull 1993;2:509–513.

Puente X, Villares R, Carral E, Carballeira A. Nacreous shellof Mytilus galloprovincialis as a biomonitor of heavy metalpollution in Galiza (NW Spain). Sci Total Environ1996;183:205–211.

Reeders HH, bij de Vaate A, Noordhuis R. Potential of thezebra mussel(Dreissena polymorpha) for water qualitymanagement. In: Nalepa TF, Schloesser DW, editors. Zebramussels: biology, impacts, and control. Boca Raton, FL:Lewis Publishers, 1993. p. 439–451.

Rice MA. Environmental impacts of shellfish aquaculture:filter feeding to control eutrophication. In: Tlusty M, Bengt-son D, Halvorson HO, Oktay S, Pearce J, Rheault Jr. RB,editors. Marine aquaculture and the environment: a meetingfor stakeholders in the northeast. Falmouth, MA: Cape CodPress, 2001.

Richardson CA, Chenery SRN, Cook JM. Assessing the historyof trace metal(Cu, Zn, Pb) contamination in the North Seathrough laser ablation-ICP-MS of horse musselModiolusmodiolus shells. Mar Ecol Prog Ser 2001;157–167.

Riemann B, Nielsen TG, Horsted SJ, Koefoed Bjoernsen P,Pock-Steen J. Regulation of phytoplankton biomass in estu-arine enclosures. Mar Ecol Prog Ser 1988;48:205–215.

Sbriz L, Aquino MR, de Rodriguez NMA, Fowler SW,Sericano JL. Levels of chlorinated hydrocarbons and tracemetals in bivalves and nearshore sediments from the Domin-ican Republic. Mar Pollut Bull 1998;36:971–979.

Segar DA, Collins JD, Riley JP. The distribution of the majorand some minor elements in marine animals; Part II Mol-luscs. J Mar Biol Assoc UK 1971;51:131–136.

Seire A, Carell B, Westermark T, Mutvei H, Bignert A. Bivalveshells as environmental archives in brackish water: elementaland radioactivity studies of EstoniaMacoma baltica shells.In: Allemand D, Cuif J, editors. Biomineralisation 93.Seventh International Symposium on Biomineralisation, vol.14 (4). Monaco: Bulletin de L’Institut Oceanographique;1996. p. 97–104.

Seki M. Studies on environmental factors for the growth ofthe pearl oyster,Pinctada fucata, and the quality of its pearlunder the culture condition. Bull Mie Pref Fish Exp Stat1972;32–143 (In Japanese with English summary andfigures).

Sericano JL, Mee LD, Readmann JW, Villeneuve J-P, WadeTL, Jackson TJ. Trace organic contamination in the Ameri-cas: an overview of the US National Status & Trends and


the International ‘Mussel Watch’ Programmes. Mar PollutBull 1995;31:214–225.

Shpigel M, Blaylock RA. The Pacific oyster,Crassostreagigas, as a biological filter for a marine fish aquaculturepond. Aquaculture 1991;92:187–197.

Sidwell VD, Bonnet JC, Zook EG. Chemical and nutritivevalues of several fresh and canned finfish, crustaceans, andmolluscs. I. Proximate composition, calcium and phospho-rous. Mar Fish Rev 1973;35:16–19.

Silverman H, Achberger EC, Lynn JW, Dietz TH. Filtrationand utilization of laboratory-cultured bacteria byDreissenapolymorpha, Corbicula fluminea, andCarunculina texasen-sis. Biol Bull 1995;187:308–319.

Smit H, bij de Vaate A, Reeders H, van Nes E, Noordhuis R.Colonization, ecology, and positive aspects of zebra mussels(Dreissena polymorpha) in The Netherlands. In: Nalepa TF,Schloesser DW, editors. Zebra mussels: biology, impacts,and control. Boca Raton, FL: Lewis Publishers, 1993. p.55–77.

Songsangjinda P, Matsuda O, Yamamoto T, Rajendran N,Maeda H. The role of suspended oyster culture on nitrogencycle in Hiroshima Bay. J Oceanogr 2000;56:223–231.

Souchu P, Vaquer A, Collos Y, Landrein S, Deslous-Paoli J-M, Bibent B. Influence of shellfish farming activities on thebiogeochemical composition of the water column in Thaulagoon. Mar Ecol Prog Ser 2001;218:141–152.

Stenton-dozey JME, Jackson LF, Busby AJ. Impact of musselculture on macrobenthic community structure in SaldanhaBay, South Africa. Mar Pollut Bull 1999;39:357–366.

Sturesson U. Lead enrichment in shells ofMytilus edulis.Ambio 1976;5:253–256.

Sturesson U. Cadmium enrichment in shells ofMytilus edulis.Ambio 1978;7:122–125.

Suzuki K. Biochemical studies on the pearl oyster(Pinctadamartensii) and its growing environments. I. The seasonalchanges in the chemical components of the pearl oyster,plankton and marine mud. Bull Nat Pearl Res Lab1957;2:57–62 (In Japanese with English summary).

Underwood AJ. Beyond BACI: the detection of environmentalimpacts on populations in the real, but variable, world. JExp Mar Biol Ecol 1992;161:145–178.

Underwood AJ. Detection and measurement of environmentalimpacts. In: Underwood AJ, Chapman MG, editors. Coastalmarine ecology of temperate Australia. Sydney, Australia:UNSW Press, 1995.

Villeneuve J-P, Carvalho FP, Fowler SW, Cattini C. Levelsand trends of PCBs, chlorinated pesticides and petroleumhydrocarbons in mussels from the NW Mediterranean coast:comparison of concentrations in 1973y1974 and 1988y1989.Sci Total Environ 1999;237–238:57–65.

Walsh K, Dunstan RH, Murdoch RN, Conroy BA, RobertsTK, Lake P. Bioaccumulation of pollutants and changes inpopulation parameters in the gastropod molluscAustrococh-lea constricta. Arch Environ Contam Toxicol 1994;26:367–373.

Walsh K, Dunstan RH, Murdoch RN. Differential bioaccu-mulation of heavy metals and organopollutants in the softtissue and shell of the marine gastropod,Austrocochleaconstricta. Arch Environ Contam Toxicol 1995;28:35–39.

Warwick R. Environmental impact studies on marine commu-nities: pragmatical considerations. Aust J Ecol 1993;18:63–80.

Westermark T, Carell B, Forberg S, Mutvei H, Kulakowski E.Freshwater unionid(Mollusca: Bivalvia) shells as environ-mental archives: methodology and observations. In: Alle-mand D, Cuif J, editors. Biomineralisation 93. SeventhInternational Symposium on Biomineralisation, vol. 14(4).Monaco: Bulletin de L’Institut Oceanographique; 1996. p.73–81.

Westermark T, Carell B, Mutvei M, Forberg S, Kulakowski E.Elemental content in shells of the ocean quahog,Arcticaislandica L. (Mollusca: Bivalvia), from NW Europe asmarine environmental archives. In: Allemand D, Cuif J,editors. Biomineralisation 93. Seventh International Sym-posium on Biomineralisation, vol. 14(4). Monaco: Bulletinde L’Institut Oceanographique; 1996. p. 105–111.

Wiesner L, Gunther B, Fenske C. Temporal and spatialvariability in the heavy-metal content ofDreissena poly-morpha (Pallas) (Mollusca: Bivalvia) from the Kleines Haff(northeastern Germany). Hydrobiologia 2001;443:137–145.

Yamamuro M, Hiratsuka J, Ishitobi Y. Seasonal change in afilter-feeding bivalveMusculista senhousia population of aeutrophic lagoon. J Mar Sys 2000;26:117–126.

pearl aquaculture—profitable environmental remediation?

Documents